Effects of iron oxide nanoparticles on phenotype and metabolite changes in hemp clones (Cannabis sativa L.)

Canhui Deng, Qing Tang, Zemao Yang, Zhigang Dai, Chaohua Cheng, Ying Xu, Xiaojun Chen, Xiaoyu Zhang, Jianguang Su

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Front. Environ. Sci. Eng. ›› 2022, Vol. 16 ›› Issue (10) : 134. DOI: 10.1007/s11783-022-1569-9
RESEARCH ARTICLE
RESEARCH ARTICLE

Effects of iron oxide nanoparticles on phenotype and metabolite changes in hemp clones (Cannabis sativa L.)

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Highlights

● Fe3O4 NPs increased the biomass and chlorophyll content of hemp clones.

● Fe3O4 NPs penetrated and were internalized by root cells.

● Fe3O4 NPs induced the alteration of metabolite profiles in hemp leaves.

● The psychoactive compound THC in hemp leaves was significantly down-regulated.

Abstract

We investigated the effect of iron oxide nanoparticles (Fe3O4 NPs, ~17 nm in size) on the phenotype and metabolite changes in hemp (Cannabis sativa L.), an annual crop distributed worldwide. Hemp clones were grown in hydroponic cultures with Fe3O4 NPs (50, 100, 200, or 500 mg/L) for four weeks. TEM and ICP-MS were used to determine Fe3O4 NPs uptake and translocation. LC-MS-based metabolomics was employed to explore the deep insight into the effect of Fe3O4 NPs on hemp plants. The results revealed that plant growth enhanced gradually with increasing concentrations of given NPs up to 200 mg/L, which improved the fresh weight and dry weight by 36.13% and 74.68%, respectively, compared to the control. Even at a high dose (500 mg/L), Fe3O4 NPs promoted plant growth, including increased biomass and tissue length. NPs significantly increased the iron and chlorophyll content in plant tissues Increased catalase activity and reduced hydrogen peroxide content in hemp leaves suggested that the Fe3O4 NPs activated the defense system. TEM showed that NPs were abundantly attached to the cell wall and dispersed throughout the root cells. Metabolomics revealed that Fe3O4 NPs induced metabolic reprogramming in hemp leaves, including the up-regulation of carbohydrates and organic acids, and down-regulation of antioxidants, especially tetrahydrocannabinol (THC). The significantly up-regulated metabolites, including peonidin and 2-hydroxycinnamic acid, could be involved in photosynthesis in hemp plants. These results demonstrate the potential of Fe3O4 NPs for promoting hemp growth and decreasing the THC content at low doses.

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Keywords

Fe3O4 nanoparticle / Hemp / Growth enhancement / THC / Metabolite

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Canhui Deng, Qing Tang, Zemao Yang, Zhigang Dai, Chaohua Cheng, Ying Xu, Xiaojun Chen, Xiaoyu Zhang, Jianguang Su. Effects of iron oxide nanoparticles on phenotype and metabolite changes in hemp clones (Cannabis sativa L.). Front. Environ. Sci. Eng., 2022, 16(10): 134 https://doi.org/10.1007/s11783-022-1569-9

References

[1]
Agrawal B , Lakshmanan V , Kaushik S , Bais H P . (2012). Natural variation among Arabidopsis accessions reveals malic acid as a key mediator of Nickel (Ni) tolerance. Planta, 236( 2): 477– 489
CrossRef Google scholar
[2]
Al-Amri N , Tombuloglu H , Slimani Y , Akhtar S , Barghouthi M , Almessiere M , Alshammari T , Baykal A , Sabit H , Ercan I , Ozcelik S . (2020). Size effect of iron (III) oxide nanomaterials on the growth, and their uptake and translocation in common wheat (Triticum aestivum L.). Ecotoxicology and Environmental Safety, 194 : 110377
CrossRef Google scholar
[3]
Atak Q, Celik O, Olgun A, Alikamanoglu S, Rzakoulieva A ( 2007). Effect of magnetic field on peroxidase activities of soybean tissue culture.Biotechnology, Biotechnological Equipment, 21( 2): 166− 171
[4]
Bar-Sela G , Vorobeichik M , Drawsheh S , Omer A , Goldberg V , Muller E . (2013). The medical necessity for medicinal cannabis: prospective, observational study evaluating the treatment in cancer patients on supportive or palliative care. Evidence-based complementary and alternative medicine: eCAM, 2013 : 1– 8
CrossRef Google scholar
[5]
Barhoumi L , Oukarroum A , TaherL B , SmiriL S , Abdelmelek H , Dewez D . (2015). Effects of superparamagnetic iron oxide nanoparticles on photosynthesis and growth of the aquatic plant Lemna gibba. Archives of Environmental Contamination and Toxicology, 68( 3): 510– 520
CrossRef Google scholar
[6]
Borges R S, Batista J Jr, Viana R B, Baetas A C, Orestes E, Andrade M A, Honório K M, da Silva A B F ( 2013). Understanding the molecular aspects of tetrahydrocannabinol and cannabidiol as antioxidants. Molecules (Basel, Switzerland), 18( 10): 12663− 12674
Pubmed
[7]
Cai L , Cai L , Jia H , Liu C , Wang D , Sun X . (2020). Foliar exposure of Fe3O4 nanoparticles on Nicotiana benthamiana: Evidence for nanoparticles uptake, plant growth promoter and defense response elicitor against plant virus. Journal of Hazardous Materials, 393 : 122415
CrossRef Google scholar
[8]
Carvalho I S , Cavaco T , Carvalho L M , Duque P . (2010). Effect of photoperiod on flavonoid pathway activity in sweet potato (Ipomoea batatas (L.) Lam.). leaves. Food Chemistry, 118( 2): 384– 390
CrossRef Google scholar
[9]
Chichiriccò G, Poma A ( 2015). Penetration and toxicity of nanomaterials in higher plants. Nanomaterials (Basel, Switzerland), 5( 2): 851− 873
Pubmed
[10]
Deng J H , Zhang X R , Zeng G M , Gong J L , Niu Q Y , Liang J . (2013). Simultaneous removal of Cd(II) and ionic dyes from aqueous solution using magnetic graphene oxide nanocomposite as an adsorbent. Chemical Engineering Journal, 226 : 189– 200
CrossRef Google scholar
[11]
Feyissa B A , Arshad M , Gruber M Y , Kohalmi S E , Hannoufa A . (2019). The interplay between miR156/SPL13 and DFR/WD40-1 regulate drought tolerance in alfalfa. BMC Plant Biology, 19( 1): 434– 453
CrossRef Google scholar
[12]
Ghafariyan M H , Malakouti M J , Dadpour M R , Stroeve P , Mahmoudi M . (2013). Effects of magnetite nanoparticles on soybean chlorophy Ⅱ. Environmental Science & Technology, 47( 18): 10645– 10652
CrossRef Google scholar
[13]
Hu J , Wu X Y , Wu F , Chen W X , Zhang X Y , White J C , Li J L , Wan Y , Liu J F , Wang X L . (2020). TiO2 nanoparticle exposure on lettuce (Lactuca sativa L.):. Dose-dependent deterioration of nutritional quality. Environmental Science-Nano, 7( 2): 501– 513
CrossRef Google scholar
[14]
Júnior A L G , Islam M T , Nicolau L A D , de Souza L K M , Araújo T D S , Lopes de Oliveira G A , de Melo Nogueira K , da Silva Lopes L , Medeiros J R , Mubarak M S , Melo-Cavalcante A A C . (2020). Anti-Inflammatory, antinociceptive, and antioxidant properties of anacardic acid in experimental models. ACS Omega, 5( 31): 19506– 19515
CrossRef Google scholar
[15]
Kim J H , Lee Y , Kim E J , Gu S , Sohn E J , Seo Y S , An H J , ChangY S . (2014). Exposure of iron nanoparticles to Arabidopsis thaliana enhances root elongation by triggering cell wall loosening. Environmental Science & Technology, 48( 6): 3477– 3485
CrossRef Google scholar
[16]
Labille J , Catalano R , Slomberg D , Motellier S , Pinsino A , Hennebert P , Santaella C , Bartolomei V . (2020). Assessing sunscreen lifecycle to minimize environmental risk posed by nanoparticulate uv-filters: A review for safer-by design products. Frontiers in Environmental Science, 8 : 1– 25
CrossRef Google scholar
[17]
Li J , Hu J , Ma C , Wang Y , Wu C , Huang J , Xing B . (2016a). Uptake, translocation and physiological effects of magnetic iron oxide (gamma-Fe2O3) nanoparticles in corn (Zea mays L.). Chemosphere, 159 : 326– 334
CrossRef Google scholar
[18]
Li J , Hu J , Xiao L , Wang Y , Wang X . (2018). Interaction mechanisms between α-Fe2O3, γ-Fe2O3 and Fe3O4 nanoparticles and Citrus maxima seedlings. Science of the Total Environment, 625 : 677– 685
CrossRef Google scholar
[19]
Li P Y , Wang A D , Du W C , Mao L , Wei Z B , Wang S F , Yuan H Y , Ji R , Zhao L J . (2020). Insight into the interaction between Fe-based nanomaterials and maize (Zea mays) plants at metabolic level. Science of the Total Environment, 738 : 139795– 139804
CrossRef Google scholar
[20]
Liu Y H , Offler C E , Ruan Y L . (2014). A simple, rapid, and reliable protocol to localize hydrogen peroxide in large plant organs by DAB-mediated tissue printing. Frontiers in Plant Science, 5 : 1– 6
CrossRef Google scholar
[21]
Li Y , Niu J , Shang E , Crittenden J C . (2016b). Influence of dissolved organic matter on photogenerated reactive oxygen species and metal-oxide nanoparticle toxicity. Water Research, 98 : 9– 18
CrossRef Google scholar
[22]
Lo Piccolo E , Landi M , Massai R , Remorini D , Guidi L . (2020). Girled-induced anthocyanin accumulation in red-leafed Prunus cerasifera: Effect on photosynthesis, photoprotection and sugar metabolism. Plant Science:An International Journal of Experimental Plant Biology, 294 : 110456
CrossRef Google scholar
[23]
Lu A , Li Y , Ding H , Xu X , Li Y , Ren G , Liang J , Liu Y , Hong H , Chen N , Chu S , Liu F , Li Y , Wang H , Ding C , Wang C , Lai Y , Liu J , Dick J , Liu K , Hochella M F Jr . (2019). Photoelectric conversion on Earth’s surface via widespread Fe- and Mn-mineral coatings. Proceedings of the National Academy of Sciences of the United States of America, 116( 20): 9741– 9746
CrossRef Google scholar
[24]
Morales M I , Rico C M , Hernandez-Viezcas J A , Nunez J E , Barrios A C , Tafoya A , Flores-Marges J P , Peralta-Videa J R , Gardea-Torresdey J L . (2013). Toxicity assessment of cerium oxide nanoparticles in cilantro (Coriandrum sativum L). plants grown in organic soil. Journal of Agricultural and Food Chemistry, 61( 26): 6224– 6230
CrossRef Google scholar
[25]
Pariona N , Martínez A I , Hernandez-Flores H , Clark-Tapia R . (2017). Effect of magnetite nanoparticles on the germination and early growth of Quercus macdougallii. Science of the Total Environment, 575 : 869– 875
CrossRef Google scholar
[26]
Parisi C, Vigani M, Rodriguez-Cerezo E ( 2015). Agricultural nanotechnologies: What are the current possibilities? Nano Today, 10( 2): 124− 127
[27]
Rico C M , Majumdar S , Duarte-Gardea M , Peralta-Videa J R , Gardea-Torresdey J L . (2011). Interaction of nanoparticles with edible plants and their possible implications in the food chain. Journal of Agricultural and Food Chemistry, 59( 8): 3485– 3498
CrossRef Google scholar
[28]
Schluttenhofer C , Yuan L . (2017). Challenges towards revitalizing hemp: A multifaceted crop. Trends in Plant Science, 22( 11): 917– 929
CrossRef Google scholar
[29]
Senge M O , Ryan A A , Letchford K A , MacGowan S A , Mielke T . (2014). Chlorophylls, symmetry, chirality, and photosynthesis. Symmetry, 6( 3): 781– 843
CrossRef Google scholar
[30]
Tombuloglu H , Anıl I , Akhtar S , Turumtay H , Sabit H , Slimani Y , Almessiere M , Baykal A . (2020). Iron oxide nanoparticles translocate in pumpkin and alter the phloem sap metabolites related to oil metabolism. Scientia Horticulturae, 265 : 109223
CrossRef Google scholar
[31]
Tombuloglu H , Slimani Y , Tombuloglu G , Almessiere M , Baykal A . (2019a). Uptake and translocation of magnetite (Fe3O4) nanoparticles and its impact on photosynthetic genes in barley (Hordeum vulgare L). Chemosphere, 226 : 110– 122
CrossRef Google scholar
[32]
Tombuloglu H, Slimani Y, Tombuloglu G, Almessiere M, Baykal A, Ercan I, Sozeri H( 2019b). Tracking of NiFe2O4 nanoparticles in barley ( Hordeum vulgare L.) and their impact on plant growth, biomass, pigmentation, catalase activity, and mineral uptake . Environmental Nanotechnology, Monitoring & Management, 11: 100223
[33]
Wang H , Kou X , Pei Z , Xiao J Q , Shan X , Xing B . (2011). Physiological effects of magnetite (Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne L. ) and pumpkin (Cucurbita mixta) plants. Nanotoxicology, 5( 1): 30– 42
CrossRef Google scholar
[34]
Xu J , Sun J , Du L , Liu X . (2012). Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytologist, 196( 1): 110– 124
CrossRef Google scholar
[35]
Xu Y , Qin Y , Palchoudhury S , Bao Y . (2011). Water-soluble iron oxide nanoparticles with high stability and selective surface functionality. Langmuir, 27( 14): 8990– 8997
CrossRef Google scholar

Acknowledgements

This research was supported by the Natural Science Foundation of Hunan Province of China (No. 2020JJ5643), and the National Natural Science Foundation of China (No. 31770341).

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2022 Higher Education Press
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